Widespread Prevalence of Wolbachia in Laboratory Stocks and the Implications for Drosophila Research

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Wolbachia is an intracellular microbe harbored by a wide variety of arthropods (including Drosophila) and filarial nematodes. Employing several different strategies including male killing, induced parthenogenesis, cytoplasmic incompatibility, and feminization, and acting by as-yet-unknown mechanisms, Wolbachia alters host reproduction to increase its representation within a population. Wolbachia is closely associated with gametic incompatibility but also interacts with Drosophila in other, little understood ways. We report here significant and widespread infection of Wolbachia within laboratory stocks and its real and potential impact on Drosophila research. We describe the results of a survey indicating that ~30% of stocks currently housed at the Bloomington Drosophila Stock Center are infected with Wolbachia. Cells of both reproductive tissues and numerous somatic organs harbor Wolbachia and display considerable variation in infection levels within and between both tissue types. These results are discussed from the perspective of Wolbachia's potential confounding effects on both host fitness and phenotypic analyses. In addition to this cautionary message, the infection status of stock centers may provide further opportunities to study the genetic basis of host/symbiosis.

WOLBACHIA is an intracellular microbe harbored by a wide variety of arthropod and filarial nematode hosts. During studies of reproductive isolation in Culex pipiens, a rickettsia-like microorganism, Wolbachia pipientisVfns determined to be the agent responsible for a form of inherited reproductive failure (LAVEN 1959; YEN and BARR 1973). This phenotype, termed cytoplasmic incompatibility (CI), is manifestwhen a Wolbachiainfected male mates with an uninfected female (Figure 1) or with a female infected with a different Wolbachia type. In addition to Diptera, CI has since been found to be a Wolbachia-induced trait in a wide diversity of arthropod orders, including Acarina (VELA et al. 2000), Coleoptera (WADE and STEVENS 1985), Homoptera (HOSHIZAKI and SHIMADA 1995), Hymenoptera (BREEUWERand WERREN 1990), Isoptera (BANDI etal. 1997), Lepidoptera (BROWER 1976), and Orthoptera (KAMODA etal. 2000). Since all Wolbachia are removed from spermatids prior to the completion of spermatogenesis (BRESSAC and ROUSSET 1993; SNOOK et al. 2000; CLARK et al. 2002), Wolbachia presumably modify sperm prior to the completion of spermatogenesis. The transfer and processing of at least two accessory gland proteins (Acp26Aa and Acp36De) is unaffected by Wolbachia (SNOOK et al. 2000), again suggesting that the primary effect is on sperm. The CI phenotype seen in incompatible embryos in Drosophila melanogaster (Figure 1) as well as in D. simulons (O'NEILL and KARR 1990; CALLAINI et al. 1996; LASSY and KARR 1996), C. pipiens (JOST 1970), Armadillidium vulgare (MORET et al. 2001), and Nasonia vitripennis (REED and WERREN 1995) is characterized by asynchronous mitotic divisions and chromatin bridges between nuclei, defects that accumulate with subsequent mitotic divisions, resulting in embryo lethality. The earliest CI defect, observed in both Nasonia and Drosophila, is delayed paternal pronuclear breakdown and entry into mitosis (REED and WERREN 1995; CALLAINI et al. 1997; TRAM and SULLIVAN 2002).

In addition to CI, Wolbachia has been found to manipulate host reproduction in other ways, including feminization, male killing, and parthenogenesis. Each of these Wolbachia-induced phenotypes serves the same purpose: to increase the prevalence of Wolbachia-infected individuals (STOUTHAMER et al. 1999). Although CI is by far the most prevalent effect of Wolbachia infection in Drosophila, male-killing Wolbachia have recently been described in Drosophila although their prevalence within this group has yet to be established (HuRST et al. 2000; JAENIKE et al 2003).

Wolbachia has also been found in a number of filarial nematodes, many of which are pathogenic to humans. …